Prevalence and antimicrobial resistance of retail-meat-borne Salmonella in southern China during the years 2009-2016: The diversity of contamination and the resistance evolution of multidrug-resistant isolates

Abstract

Salmonella, one of the most important foodborne pathogens, can be the cause of bacterial food-borne illness and is commonly associated with the consumption of retail meat. Multidrug-resistant Salmonella isolates with high adaptability, have been responsible for many foodborne disease outbreaks. Here we present an investigation on the contamination and the antimicrobial resistance of Salmonella in retail meat obtained from supermarkets and from open markets in Guangxi, China. From the years 2009 to 2016, a total of 604 Salmonella isolates were recovered from a total of 3340 meat samples including 797 beef, 911 pork, 942 chicken and 690 duck, representing 18.08% of the samples tested. Pork was the most contaminated meat. Salmonella was detected in 322 samples from supermarkets and the positive rate of 21.03% was higher than that of 15.70% in 284 samples from open markets (P<0.05). The prevalence of Salmonella in retail meat in the summer and fall months: June (2015, 40.63%), October (2012, 34.6%; 2016, 43.75%) was higher than in other seasons of the year. One hundred and twenty-seven serotypes were identified among the 604 Salmonella enterica isolates, and S. Derby (28.48%), S. Agona (9.77%), S. London (4.97%) and S. Enteritidis (4.47%) were the most common serotypes. Tests of susceptibility to 21 antimicrobial agents showed that 87.58% of the isolates were resistant to at least one antimicrobial, and 57.79% exhibited multidrug resistance (MDR), as they were resistant to at least three antimicrobials. The presence of most of the antimicrobial-resistant genes tested was consistent with the resistant phenotypes found. Among all the antimicrobial resistant genes (ARGs) examined in this study, bla_TEM-1, aadA1, cmlA, tetA, sul1 and sul2 were the most prevalent resistant genes in the multidrug resistant isolates. Our findings show that there was a trend that the Salmonella contamination in retail meat had increased and isolates showed an MDR phenotype and that the MDR had become more and more serious. Twenty-one isolates of S. Agona were randomly analyzed by using the enterobacterial repetitive intergenic consensus sequence PCR (ERIC-PCR) and six different types were found, indicating the existence of cross-contamination in the food market. The results indicate that the hazard analysis of the critical control points (HACCP) system for the whole food chain of retail meat should be further analyzed and improved.

Keywords: Amikacin (PubChem CID: 37768); Amoxicillin (PubChem CID: 33613); Ampicillin (PubChem CID: 6249); Antimicrobial resistant gene (ARG); Aztreonam (PubChem CID: 5742832); Cefazolin (PubChem CID: 33255); Cefotaxime (PubChem CID: 5742673); Ceftazidime (PubChem CID: 5481173); Ceftriaxone (PubChem CID: 5479530); Chloramphenicol (PubChem CID: 5959); Ciprofloxacin (PubChem CID: 2764); Food safety; Furazolidone (PubChem CID: 5323714); Gentamicin (PubChem CID: 3467); Hazard analysis of critical control points (HACCP); Kanamycin (PubChem CID: 6032); Methoxypyrimidine (PubChem CID: 136730); Multidrug resistance (MDR); Nalidixic acid (PubChem CID: 4421); Nitrofurantoin (PubChem CID: 6604200); Salmonella; Serotype; Spectinomycin (PubChem CID: 15541); Streptomycin (PubChem CID: 19649); Sulfaisoxazole (PubChem CID: 5344); Tetracycline (PubChem CID: 54675776).